Allelic variation in the Arabidopsis TNL CHS3/CSA1 immune receptor pair reveals two functional cell-death regulatory modes

Yu Yang; Nak Hyun Kim; Volkan Cevik; Pierre Jacob; Li Wan; Oliver J. Furzer; Jeffery L. Dangl

doi:10.1016/j.chom.2022.09.013

Allelic variation in the Arabidopsis TNL CHS3/CSA1 immune receptor pair reveals two functional cell-death regulatory modes

Yu Yang, Nak Hyun Kim, Volkan Cevik, Pierre Jacob, Li Wan, Oliver J. Furzer, Jeffery L. Dangl

Department of Life Sciences

University of North Carolina

Research output: Contribution to journal › Article › peer-review

19 Citations (SciVal)

Abstract

Some plant NLR immune receptors are encoded in head-to-head “sensor-executor” pairs that function together. Alleles of the NLR pair CHS3/CSA1 form three clades. The clade 1 sensor CHS3 contains an integrated domain (ID) with homology to regulatory domains, which is lacking in clades 2 and 3. In this study, we defined two cell-death regulatory modes for CHS3/CSA1 pairs. One is mediated by ID domain on clade 1 CHS3, and the other relies on CHS3/CSA1 pairs from all clades detecting perturbation of an associated pattern-recognition receptor (PRR) co-receptor. Our data support the hypothesis that an ancestral Arabidopsis CHS3/CSA1 pair gained a second recognition specificity and regulatory mechanism through ID acquisition while retaining its original specificity as a “guard” against PRR co-receptor perturbation. This likely comes with a cost, since both ID and non-ID alleles of the pair persist in diverse Arabidopsis populations through balancing selection.

Original language	English
Pages (from-to)	1701-1716.e5
Journal	Cell Host and Microbe
Volume	30
Issue number	12
Early online date	17 Oct 2022
DOIs	https://doi.org/10.1016/j.chom.2022.09.013
Publication status	Published - 14 Dec 2022

Bibliographical note

Funding Information:
We thank Sarah Grant, Farid El-Kasmi, and Marc T. Nishimura for excellent suggestions and comments and Jia Li for providing the bak1-3 bkk1-1 seeds. Supported by National Science Foundation (grant IOS-1758400 to J.L.D.) and HHMI . J.L.D. is a Howard Hughes Medical Institute (HHMI) Investigator. N.H.K. was partially supported by Basic Science Research Program through the National Research Foundation of Korea Fellowship funded by the Ministry of Education ( 2014R1A6A3A03058629 ). This article is subject to HHMI’s Open Access to Publications policy. HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the author-accepted manuscript of this article can be made freely available under a CC BY4.0 license immediately upon publication.

Keywords

BAK1
CHS3
co-evolution
CSA1
guard hypothesis
paired NLR
plant immune system
specialization

ASJC Scopus subject areas

Parasitology
Microbiology
Virology

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10.1016/j.chom.2022.09.013Licence: CC BY

Cite this

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title = "Allelic variation in the Arabidopsis TNL CHS3/CSA1 immune receptor pair reveals two functional cell-death regulatory modes",

abstract = "Some plant NLR immune receptors are encoded in head-to-head “sensor-executor” pairs that function together. Alleles of the NLR pair CHS3/CSA1 form three clades. The clade 1 sensor CHS3 contains an integrated domain (ID) with homology to regulatory domains, which is lacking in clades 2 and 3. In this study, we defined two cell-death regulatory modes for CHS3/CSA1 pairs. One is mediated by ID domain on clade 1 CHS3, and the other relies on CHS3/CSA1 pairs from all clades detecting perturbation of an associated pattern-recognition receptor (PRR) co-receptor. Our data support the hypothesis that an ancestral Arabidopsis CHS3/CSA1 pair gained a second recognition specificity and regulatory mechanism through ID acquisition while retaining its original specificity as a “guard” against PRR co-receptor perturbation. This likely comes with a cost, since both ID and non-ID alleles of the pair persist in diverse Arabidopsis populations through balancing selection.",

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author = "Yu Yang and Kim, {Nak Hyun} and Volkan Cevik and Pierre Jacob and Li Wan and Furzer, {Oliver J.} and Dangl, {Jeffery L.}",

note = "Funding Information: We thank Sarah Grant, Farid El-Kasmi, and Marc T. Nishimura for excellent suggestions and comments and Jia Li for providing the bak1-3 bkk1-1 seeds. Supported by National Science Foundation (grant IOS-1758400 to J.L.D.) and HHMI . J.L.D. is a Howard Hughes Medical Institute (HHMI) Investigator. N.H.K. was partially supported by Basic Science Research Program through the National Research Foundation of Korea Fellowship funded by the Ministry of Education ( 2014R1A6A3A03058629 ). This article is subject to HHMI{\textquoteright}s Open Access to Publications policy. HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the author-accepted manuscript of this article can be made freely available under a CC BY4.0 license immediately upon publication. ",

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AU - Wan, Li

AU - Furzer, Oliver J.

AU - Dangl, Jeffery L.

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Allelic variation in the Arabidopsis TNL CHS3/CSA1 immune receptor pair reveals two functional cell-death regulatory modes

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

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